Spontaneous vocal coordination of vocalizations to water noise in rooks (Corvus frugilegus): An exploratory study

Abstract The ability to control one's vocal production is a major advantage in acoustic communication. Yet, not all species have the same level of control over their vocal output. Several bird species can interrupt their song upon hearing an external stimulus, but there is no evidence how flexible this behavior is. Most research on corvids focuses on their cognitive abilities, but few studies explore their vocal aptitudes. Recent research shows that crows can be experimentally trained to vocalize in response to a brief visual stimulus. Our study investigated vocal control abilities with a more ecologically embedded approach in rooks. We show that two rooks could spontaneously coordinate their vocalizations to a long‐lasting stimulus (the sound of their small bathing pool being filled with a water hose), one of them adjusting roughly (in the second range) its vocalizations as the stimuli began and stopped. This exploratory study adds to the literature showing that corvids, a group of species capable of cognitive prowess, are indeed able to display good vocal control abilities.


| INTRODUC TI ON
Vocal production is an important feature of animal communication and its functions are as diverse as territory defense, courtship, or exchange of information (Chen & Wiens, 2020). Vocal control is the ability to modify elements of an ongoing vocal output (Miller et al., 2003) and it undeniably confers benefits to birds as it enables them to adapt their response according to external stimuli.
For example, birds can interrupt their vocalization upon hearing a predator approaching or match their neighbor's song when engaging in vocal competition (Beecher et al., 2000;Mougeot & Bretagnolle, 2000;Schmidt & Belinsky, 2013). This ability can include volitional processes, but also other types of involuntary processes like affective (emotional) processes (Hopf et al., 1992;Nieder & Mooney, 2019). Indeed, changes in the level of arousal can trigger the modulations of a call. The wide diversity of species using vocal communication also implies a broad spectrum of vocal control (Miller et al., 2003). Note that it seems unlikely that a species could have no control whatsoever over its vocal production. There should be some species with little control at one end of the spectrum, that is, the vocal output cannot be modulated once it has begun, whilst the other end of the spectrum should feature species with high levels of vocal control that are able to modify the individual elements (such as syllables) of a vocalization (Miller et al., 2003).
Vocal control has been investigated in a diversity of species (bats, Smotherman, 2007;budgerigars, Osmanski & Dooling, 2009;anurans, Cunnington & Fahrig, 2010;pinnipeds, Torres Borda et al., 2021; monkeys, Hage et al., 2013Hage et al., , 2016Hage & Nieder, 2015;Gavrilov & Nieder, 2021), but most studies have focused on songbirds and the neuronal circuitry underpinning their songs (Brenowitz, 2004;Keller & Hahnloser, 2009;Konishi, 1985). Some species can change the duration or the average pitch of their vocalizations, and also the timing, number, arrangement, and structure of syllables or other basic units (Brumm, 2006;Carlson et al., 2020;Slabbekoorn & Peet, 2003;Templeton et al., 2005;Villain et al., 2016). They can also modulate the intensity of the vocalization, which has been shown in several bird species (The Lombard effect, i.e., a modification of the vocal output to compensate for surrounding noise) (Brumm et al., 2009;Brumm & Todt, 2002;Luo et al., 2018;Manabe et al., 1998). Previous researchers have also used interruptibility experiments, which detect the ability of an individual to interrupt its song in response to an external acoustic stimulus. Heuglin's robins (Todt, 1971), blackbirds (Todt, 1975), nightingales (Hultsch & Todt, 1982), Bengalese finches (Seki et al., 2008), and chaffinches (Heymann & Bergmann, 1988) can interrupt their songs upon hearing a noise. Several species can also interrupt their vocalizations in response to a non-acoustic stimulus (e.g., light flash stimulations). This has been shown in zebra finches (Cynx, 1990) and nightingales (Riebel & Todt, 1997), but also in doves (ten Cate & Ballintijn, 1996), which are not songbirds. Interestingly, the subjects in these experiments often completed the ongoing syllable before stopping (Cynx, 1990). Doves were not always able to interrupt an ongoing vocal element if the flash occurred early during the element (ten Cate & Ballintijn, 1996). These experiments provide some evidence of vocal control and show the limits of this control over the production of vocalizations. In a recent study (Brecht et al., 2019), two crows were experimentally trained to emit a call following the appearance of a Go-visual cue. They started vocalizing within 2-3 s of the stimulus presentation and did not vocalize when a No-Go-cue was shown. The authors argue that crows were capable of volitional control over the onset of their vocalizations (Brecht et al., 2019), as their calls were not triggered by affective (and involuntary) processes. Although volitional control has been studied in monkeys (Coudé et al., 2011;Ghazanfar et al., 2019;Hage et al., 2013), the large number of studies on vocal control has shown very little interest in the volitional aspects of vocalizations in other species, and particularly birds. More generally, the notion remains difficult to demonstrate, as it requires a clear demonstration of the dissociation between emotional and non-emotional control of the vocalizations.
Still, it could be hypothesized that species with advanced cognitive performances have greater control of their vocal output.
Very few studies have assessed the connection between non-vocal cognitive skills and vocal production in songbirds. A study on song sparrows seems to indicate that the size of the song repertoire may correlate with performances in a detour reaching task (Boogert et al., 2011; but see also DuBois et al., 2018 for opposite results).
However, song repertoire size does not correlate with other cognitive measures (Boogert et al., 2011). More generally, intra-species performances in birds do not always correlate from one cognitive task to another (Boogert et al., 2011). However, one group of species has been extensively studied for their social and physical cognitive skills and shows good and consistent cognitive performances in a large diversity of cognition tests: the corvids (Lefebvre et al., 2004).
Corvids are technically songbirds, but they have not received much attention in acoustic studies compared to other species of songbirds.
Described as "songbirds without songs" (Fitch & Bugnyar, 2015), they emit a series of vocalizations that are sometimes produced in no particular context (Brown, 1985;Marler, 2004). They have also been anecdotally reported to imitate human voices in the same way that parrots do and can produce duetting behavior Kondo et al., 2010;Reber et al., 2016). They have excellent learning, memory, and planning skills, show long-term vocal recognition of congeners, and have sophisticated social cognitive skills (Boeckle & Bugnyar, 2012;Bugnyar et al., 2016;Emery, 2004;Emery et al., 2007;Güntürkün & Bugnyar, 2016;Raby et al., 2007). They also appear to have the same neural song system as other oscines (Kersten et al., 2021;Wang et al., 2009). We can, thus, expect them to have good control over their vocal production as suggested by the crow study in Brecht et al. (2019).
This study investigates vocal control in another species of corvids, the rook (Corvus frugilegus). We had previously observed that certain birds in a captive colony of 14 adult rooks would spontaneously produce long series of different vocal elements (squawks, sneezes, snores, or cackles), sometimes upon hearing loud noise, such as engine noises like passing planes or motorbikes (Video S1). Our study, thus, provides complementary data on corvids vocal control with a more ecologically embedded approach.

| Subjects
The studied group was housed on the CNRS campus of Cronenbourg in Strasbourg, France. Ten of these birds were collected from a wild local colony after they fell from the nest. They were then raised together and handfed by humans for a few weeks until they reached feeding autonomy. After a few months, they became very independent from humans, avoiding contact and staying cohesive with the other members of the group. In 2016, wild birds, collected from hunting traps, integrated the group: one was a 4-month-old immature male, and the others were adult females.
Group composition changed slightly over the duration of the study (which spanned 4 years, from 2014 to 2018), with 14 birds (9 males and 5 females) in 2014, 16 in 2016 (9 males, 7 females), and 14 in 2017 (8 males and 6 females, Table 1). Only three rooks took part in the experiment described in this study: Kafka, who is one of the highest ranking males, Tom who has an intermediary rank, and Brain who is often the lowest ranking male in the group hierarchy.
The rooks were housed in a large outdoor aviary (18 × 6 × 3.5 m) containing wooden perches, platforms, suspended baskets, ropes, vegetation cover, and branches, as well as two small water pools for enrichment and bathing. Individuals were fed daily with a mixture of pellets and fresh products (eggs, yoghurt, and fruit) and had ad libitum access to water. All birds were easily identifiable through colored leg rings.

| General procedure
The tests took place at the normal time of the daily aviary cleaning routine. Thus, one of the bathing pools was first emptied, scrubbed, and then rinsed by the experimenter, as carried out in the usual daily routine. The bathing pool was a small plastic recipient in the form of a seashell (75 × 85 × 25 cm). The cleaning of the pool lasted approximately 30 s to a minute. The main experimenter then stood still, holding a water hose (to fill up the pool), a chronometer, and a list of phase durations for the filling and pause phases ( Figure 1). The experimenter was never looking toward the birds to avoid inadvertently providing them with cues.
All test sessions were conducted in a group setting, and all members of the group were free to join the experiment (i.e., vocalize).
However, we focused on the first bird who vocalized (hereinafter referred to as the first singer) to investigate potential coordination with the noise. Note that other birds could also vocalized, but given that it was not possible for us to decipher if they were then reacting to the stimulus or to the vocalizations of the first singer, we chose not to record their behavior and focused the camera on the first singer only. Test sessions always started with the first 20-s phase of water filling of the pool, to signal the beginning of the experiment to the birds ( Figure 2). The experimenter then continued the session with alternate phases of fillings, which produced a water noise, and pauses. These phases of filling and pauses will hereafter be referred to as "phases". Phases of filling and pauses lasted 5, 10, 15, or 20 s.
The durations of the phases following the initial filling were randomly determined before the experiment so that they could not be predicted by the birds. An observer sat quietly in a corner of the aviary without moving, holding a camera, and looking down at the screen of the camera, filming the first bird that vocalized. In some rare circumstances, a bird could stop vocalizing after only a few phases. If another bird then started to vocalize, it became the new focal individual (hereinafter referred to as the second singer) and was subsequently filmed for the whole duration of the session (this occurred only twice). Note that we had no control over the duration of involvement of the birds, as they were free to vocalize or to remain silent at any time during the sessions. However, given that all birds in the enclosure could hear the sound of the water-filling noise, both primary and secondary singers that vocalized had been exposed to the same sequences of stimuli. Birds were not encouraged to come closer to the pool or vocalize in any way and were not rewarded in any way before, during, or after the session. In many sessions, no   We also analyzed "natural" series of vocalizations (Video S1) as a means of comparison with those produced in the context of the experiment. Those series of vocalizations comprised at least two different vocalization types repeated several times. They were recorded over a period of 5 years (2013-2018) and occurred outside of any experimental context. We analyzed the length of 49 series for Brain and 40 for Kafka using the software Audacity. Several series of vocalizations could be produced in a row but they were always separated by at least 2 s, a duration well above the median duration of inter-vocalization intervals (median Kafka = 0.6 s, median Brain = 0.5 s).
On average, each of Brain's "natural" series of vocalizations lasted 10.8 s without pause, while each of Kafka's lasted 12.5 s.

| Statistics
We first examined the proportion of vocalizing events that occurred during fillings versus pauses using a binomial exact test (null hypothesis set at 50%, "stats" package in R) for the singers. As the birds rather than on the duration of the pause. To investigate this question, we ran a linear mixed effect model to test the effect of the interaction of the "duration of phases" and the type of phase (filling or pauses) as fixed effects on the "duration of vocalisations" as the response variable, with the "session" variable used as a random factor (Function "lmer" in R package lme4 v.1.1-13, Bates et al., 2015). We evaluated the statistical significance of our model compared to a null model lacking all set of tested predictors using a likelihood ratio test (function "ANOVA", package "stats" in R). Post-hoc analyses were conducted using a Bonferroni correction (function "lsmeans", in R package LSmeans, Lenth, 2016). It must be noted here that the duration of each phase depended on the manual activation of the hose by the experimenter, meaning that phases could be slightly longer or shorter than the intended duration (93.8% of the filling phases were of the intended duration ± 2 s, 95.6% of the pause phases were of the intended duration ± 2 s). For this reason, the "duration of phases" variable is not implemented as a categorical variable in the analysis, but as a continuous variable with the exact durations. Adopting the same criterion as that used by Brecht et al. (2019), advanced vocal control also implies that individuals should, respectively, start and stop vocalizing within 3 s after the beginning and the end of the filling stimulus. We report the median latency of starting and stopping vocalizing after the beginning and the end of the stimulus, respectively.
Finally, we also used a linear mixed effect model to investigate whether the "duration of the vocalisation" (fixed effect) had an effect on the "latencies to stop vocalising" after the end of the filling phase (response variable), with the "session" variable used as a random factor. This model was also compared to a null model. The alpha level was set to 0.05.

| DISCUSS ION
At the group level, most birds did not react to the stimulus. However, on frequent occasions, two rooks were able to adjust roughly (within attributing an affective value to the stimulus, and their response was a learned vocalization that is not part of their standard repertoire. Our study differs strongly from Brecht et al. (2019), as we did not use any operant conditioning procedure, and the stimulus was never associated with food. Contrary to them, we cannot guarantee that the stimulus was deprived of affective meaning.
Rooks sang spontaneously. The filling of the pool may have some relevance for the birds, such as an anticipated pleasure to bathe, although they were never observed bathing directly after the experiment. However, we think it unlikely that their response was a trained response (by associative learning or conditioning).
Indeed, few birds vocalized and they did not vocalize at every session. Their response is also not comparable to a typical alarm or food call over which they would have no control. Indeed, they re- We cannot exclude that this species likes to vocalize upon hearing loud noises, or broadband sounds as they often produce these vocalizations upon hearing passing planes. The sound of water would then not be neutral because it has interesting acoustic properties, which stimulate them to vocalize. Vocal responses to water noises have been described in other species. Male chaffinches (Fringilla coelebs) can produce "rain calls" during the reproductive season; the core function of these calls is still unknown, although they might simply be a mild alarm call and may also play a role in territoriality (Randler & Förschler, 2011). Observations that bear similarities to our rooks' behavior were made by Jane Goodall (1986), who reported rain dances and waterfall displays in chimpanzees: the sound of falling water triggers a response during which the animals pay attention and react to the stimulus (Goodall, 1986). It is very likely that our birds reacted to the acoustic properties of the stimulus. The question is the amount of control involved in these non-directed songs. In Brecht et al. (2019), the two additional criteria for volitional control were as follows: temporal contingency and an absence of response in the absence of stimulus or when another stimulus was presented. More precisely, the authors ran a control condition with no-go trials in which individuals had to refrain from vocalizing when the incorrect cue was shown. Although we could not run a Go-noGo procedure, our study provides interesting results to discuss temporal contingency, and the capacity to refrain from vocalizing in rooks. Indeed, once stimulated, the birds did not vocalize for random durations but tended to adjust to the dura-  Coombs, 1960) so the production of these series of vocalizations by rooks is not an artifact of life in captivity. One interrogation concerns the low number of individuals who could be recorded as the main singer in this study. Only three birds took the role of first or second singer. Over the years, we automatically recorded this vocalizing behavior (in absence of human experimenters). Brain, Kafka, and Tom are the three most frequent singers, which probably explains that they were the first to vocalize and become the primary singers on which we focused the camera. Note also that rooks tend to sing on their own, they usually go away from the colony, perch high, and produce these series of vocalizations that are not directed toward conspecifics (Coombs, 1960). It is possible that when a rook vocalize in such a way, others tend to listen rather than sing along.
This would explain why in most cases only one bird was singing at a time. It also explains why it was difficult to record additional birds as main singers.
The vocal repertoire of rooks is very unlike those found in most birdsong. Their calls are harsh, rarely tonal, and mostly do not have harmonics. Still, it would probably be a mistake to consider that their calls require less control or modulations than those of any other songbird species. Corvid vocalizations need to be studied in greater details and compared to other songbirds. Interruptibility experiments were used to determine the basic acoustic units of songbirds' vocalizations, for example, syllables in zebra finches (Cynx, 1990). Our study works as a kind of "reverse" interruptibility experiment, in the sense that the vocalizations were started upon the beginning of the stimulus and stopped upon its end.
Notice that most endings of the vocal output occurred within 2 s of the end of a filling phase. This latency is consistent with the one displayed by some songbirds in interruptibility experiments (Riebel & Todt, 1997).
Our hypothesis was that rooks, which have demonstrated good performances and cognitive flexibility in many social and physical cognition tasks, should be able to show vocal control. We acknowledge that our experiment is less controlled than that carried out in crows and that we had no control over the willingness of the birds to come and participate. Whether our study allows

ACK N O WLE D G E M ENTS
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Open Access funding enabled and organized by Projekt DEAL.

FU N D I N G I N FO R M ATI O N
None.

CO N FLI C T O F I NTE R E S T S TATE M E NT
None.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are available in the supplementary material of this article as .csv file. Additional information can be obtained from the corresponding author VD.